The Ca2+ sensor protein CMI1 fine tunes root development, auxin distribution and responses

Signaling cross-talks between auxin, a regulator of plant development and Ca2+, a universal second messenger have been proposed to modulate developmental plasticity in plants. However, the underlying molecular mechanisms are largely unknown. Here we report that in Arabidopsis roots, auxin elicits specific Ca2+ signaling pattern that spatially coincide with the expression pattern of auxin-regulated genes. We identified the EF-hand protein CMI1 (Ca2+ sensor Modulator of ICR1) as an interactor of the ROP effector ICR1 (Interactor of Constitutively active ROP). CMI1 is monomeric in solution, changes its secondary structure at Ca2+ concentrations ranging from 10-9 to 10-8 M and its interaction with ICR1 is Ca2+ dependent, involving a conserved hydrophobic pocket. cmi1 mutants display an increased auxin response including shorter primary roots, longer root hairs, longer hypocotyls and altered lateral root formation while ectopic expression of CMI1 induces root growth arrest and reduced auxin responses at the root tip. When expressed alone, CMI1 is localized at the plasma membrane, the cytoplasm and in nuclei. Interaction of CMI1 and ICR1 results in exclusion of CMI1 from nuclei and suppression of the root growth arrest. CMI1 expression is directly upregulated by auxin while expression of auxin induced genes is enhanced in cmi1 concomitantly with repression of auxin induced Ca2+ increases in the lateral root cap and vasculature, indicating that CMI1 represses early auxin responses. Collectively, our findings identify a crucial function of Ca2+ signaling and CMI1 in root growth and suggest an auxin-Ca2+ regulatory feedback loop that fine tunes root development.

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Mepiquat chloride promotes cotton lateral root formation by modulating plant hormone homeostasis

BMC Plant Biology ◽

10.1186/s12870-019-2176-1 ◽

2019 ◽

Vol 19 (1) ◽

Cited By ~ 3

Author(s):

Qian Wu ◽

Mingwei Du ◽

Jie Wu ◽

Ning Wang ◽

Baomin Wang ◽

...

Keyword(s):

Root Growth ◽

Root Development ◽

Lateral Root ◽

Seed Treatment ◽

Molecular Mechanisms ◽

Root Formation ◽

Lateral Root Formation ◽

Mepiquat Chloride ◽

Auxin Level ◽

Lateral Root Development

Abstract Background Mepiquat chloride (MC), a plant growth regulator, enhances root growth by promoting lateral root formation in cotton. However, the underlying molecular mechanisms of this phenomenon is still unknown. Methods In this study, we used 10 cotton (Gossypium hirsutum Linn.) cultivars to perform a seed treatment with MC to investigate lateral root formation, and selected a MC sensitive cotton cultivar for dynamic monitor of root growth and transcriptome analysis during lateral root development upon MC seed treatment. Results The results showed that MC treated seeds promotes the lateral root formation in a dosage-depended manner and the effective promotion region is within 5 cm from the base of primary root. MC treated seeds induce endogenous auxin level by altering gene expression of both gibberellin (GA) biosynthesis and signaling and abscisic acid (ABA) signaling. Meanwhile, MC treated seeds differentially express genes involved in indole acetic acid (IAA) synthesis and transport. Furthermore, MC-induced IAA regulates the expression of genes related to cell cycle and division for lateral root development. Conclusions Our data suggest that MC orchestrates GA and ABA metabolism and signaling, which further regulates auxin biosynthesis, transport, and signaling to promote the cell division responsible for lateral root formation.

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Lateral root formation and nutrients: nitrogen in the spotlight

Plant Physiology ◽

10.1093/plphys/kiab145 ◽

2021 ◽

Author(s):

Pierre-Mathieu Pélissier ◽

Hans Motte ◽

Tom Beeckman

Keyword(s):

Signaling Pathways ◽

Root System ◽

Root Development ◽

Lateral Root ◽

Molecular Mechanisms ◽

Root Formation ◽

Lateral Roots ◽

Nutrient Use Efficiency ◽

Lateral Root Formation ◽

Lateral Root Development

Abstract Lateral roots are important to forage for nutrients due to their ability to increase the uptake area of a root system. Hence, it comes as no surprise that lateral root formation is affected by nutrients or nutrient starvation, and as such contributes to the root system plasticity. Understanding the molecular mechanisms regulating root adaptation dynamics towards nutrient availability is useful to optimize plant nutrient use efficiency. There is at present a profound, though still evolving, knowledge on lateral root pathways. Here, we aimed to review the intersection with nutrient signaling pathways to give an update on the regulation of lateral root development by nutrients, with a particular focus on nitrogen. Remarkably, it is for most nutrients not clear how lateral root formation is controlled. Only for nitrogen, one of the most dominant nutrients in the control of lateral root formation, the crosstalk with multiple key signals determining lateral root development is clearly shown. In this update, we first present a general overview of the current knowledge of how nutrients affect lateral root formation, followed by a deeper discussion on how nitrogen signaling pathways act on different lateral root-mediating mechanisms for which multiple recent studies yield insights.

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Lateral Root Priming Synergystically Arises from Root Growth and Auxin Transport Dynamics

10.1101/361709 ◽

2018 ◽

Cited By ~ 2

Author(s):

Thea van den Berg ◽

Kirsten H. ten Tusscher

Keyword(s):

Cell Cycle ◽

Root Growth ◽

Lateral Root ◽

Root Formation ◽

Growth Dynamics ◽

Root Tip ◽

Cycle Duration ◽

Elongation Zone ◽

Lateral Root Formation ◽

Cell Cycle Duration

AbstractThe root system is a major determinant of plant fitness. Its capacity to supply the plant with sufficient water and nutrients strongly depends on root system architecture, which arises from the repeated branching off of lateral roots. A critical first step in lateral root formation is priming, which prepatterns sites competent of forming a lateral root. Priming is characterized by temporal oscillations in auxin, auxin signalling and gene expression in the root meristem, which through growth become transformed into a spatially repetitive pattern of competent sites. Previous studies have demonstrated the importance of auxin synthesis, transport and perception for the amplitude of these oscillations and their chances of producing an actual competent site. Additionally, repeated lateral root cap apoptosis was demonstrated to be strongly correlated with repetitive lateral root priming. Intriguingly, no single mutation has been identified that fully abolishes lateral root formation, and thusfar the mechanism underlying oscillations has remained unknown. In this study, we investigated the impact of auxin reflux loop properties combined with root growth dynamics on priming, using a computational approach. To this end we developed a novel multi-scale root model incorporating a realistic root tip architecture and reflux loop properties as well as root growth dynamics. Excitingly, in this model, repetitive auxin elevations automatically emerge. First, we show that root tip architecture and reflux loop properties result in an auxin loading zone at the start of the elongation zone, with preferential auxin loading in narrow vasculature cells. Second, we demonstrate how meristematic root growth dynamics causes regular alternations in the sizes of cells arriving at the elongation zone, which subsequently become amplified during cell expansion. These cell size differences translate into differences in cellular auxin loading potential. Combined, these properties result in temporal and spatial fluctuations in auxin levels in vasculature and pericycle cells. Our model predicts that temporal priming frequency predominantly depends on cell cycle duration, while cell cycle duration together with meristem size control lateral root spacing.

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Overexpression of OsPIN2 Regulates Root Growth and Formation in Response to Phosphate Deficiency in Rice

International Journal of Molecular Sciences ◽

10.3390/ijms20205144 ◽

2019 ◽

Vol 20 (20) ◽

pp. 5144

Author(s):

Huwei Sun ◽

Xiaoli Guo ◽

Fugui Xu ◽

Daxia Wu ◽

Xuhong Zhang ◽

...

Keyword(s):

Root Growth ◽

Growth And Development ◽

Plant Root ◽

Lateral Roots ◽

Root Hairs ◽

Phosphate Deficiency ◽

P Deficiency ◽

Auxin Distribution ◽

Seminal Roots ◽

Underlying Mechanisms

The response of root architecture to phosphate (P) deficiency is critical in plant growth and development. Auxin is a key regulator of plant root growth in response to P deficiency, but the underlying mechanisms are unclear. In this study, phenotypic and genetic analyses were undertaken to explore the role of OsPIN2, an auxin efflux transporter, in regulating the growth and development of rice roots under normal nutrition condition (control) and low-phosphate condition (LP). Higher expression of OsPIN2 was observed in rice plants under LP compared to the control. Meanwhile, the auxin levels of roots were increased under LP relative to control condition in wild-type (WT) plants. Compared to WT plants, two overexpression (OE) lines had higher auxin levels in the roots under control and LP. LP led to increased seminal roots (SRs) length and the root hairs (RHs) density, but decreased lateral roots (LRs) density in WT plants. However, overexpression of OsPIN2 caused a loss of sensitivity in the root response to P deficiency. The OE lines had a shorter SR length, lower LR density, and greater RH density than WT plants under control. However, the LR and RH densities in the OE lines were similar to those in WT plants under LP. Compared to WT plants, overexpression of OsPIN2 had a shorter root length through decreased root cell elongation under control and LP. Surprisingly, overexpression of OsPIN2 might increase auxin distribution in epidermis of root, resulting in greater RH formation but less LR development in OE plants than in WT plants in the control condition but levels similar of these under LP. These results suggest that higher OsPIN2 expression regulates rice root growth and development maybe by changing auxin distribution in roots under LP condition.

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CLE-like (CLEL) peptides control the pattern of root growth and lateral root development in Arabidopsis

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1119864109 ◽

2012 ◽

Vol 109 (5) ◽

pp. 1760-1765 ◽

Cited By ~ 95

Author(s):

L. Meng ◽

B. B. Buchanan ◽

L. J. Feldman ◽

S. Luan

Keyword(s):

Root Growth ◽

Root Development ◽

Lateral Root ◽

Lateral Root Development

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CLE-CLAVATA1 Signaling Pathway Modulates Lateral Root Development under Sulfur Deficiency

Plants ◽

10.3390/plants8040103 ◽

2019 ◽

Vol 8 (4) ◽

pp. 103 ◽

Cited By ~ 8

Author(s):

Wei Dong ◽

Yinghua Wang ◽

Hideki Takahashi

Keyword(s):

Root Development ◽

Lateral Root ◽

Molecular Mechanisms ◽

Plant Root ◽

Root System Architecture ◽

Wild Type ◽

Lateral Root Development ◽

S Deficiency ◽

Cle Peptide ◽

Plant Root System

Plant root system architecture changes drastically in response to availability of macronutrients in the soil environment. Despite the importance of root sulfur (S) uptake in plant growth and reproduction, molecular mechanisms underlying root development in response to S availability have not been fully characterized. We report here on the signaling module composed of the CLAVATA3 (CLV3)/EMBRYO SURROUNDING REGION (CLE) peptide and CLAVATA1 (CLV1) leucine-rich repeat receptor kinase, which regulate lateral root (LR) development in Arabidopsis thaliana upon changes in S availability. The wild-type seedlings exposed to prolonged S deficiency showed a phenotype with low LR density, which was restored upon sulfate supply. In contrast, the clv1 mutant showed a higher daily increase rate of LR density relative to the wild-type under prolonged S deficiency, which was diminished to the wild-type level upon sulfate supply, suggesting that CLV1 directs a signal to inhibit LR development under S-deficient conditions. CLE2 and CLE3 transcript levels decreased under S deficiency and through CLV1-mediated feedback regulations, suggesting the levels of CLE peptide signals are adjusted during the course of LR development. This study demonstrates a fine-tuned mechanism for LR development coordinately regulated by CLE-CLV1 signaling and in response to changes in S availability.

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Nitrate Induction of Primary Root Growth Requires Cytokinin Signaling in Arabidopsis thaliana

Plant and Cell Physiology ◽

10.1093/pcp/pcz199 ◽

2019 ◽

Vol 61 (2) ◽

pp. 342-352 ◽

Cited By ~ 5

Author(s):

Pamela A Naulin ◽

Grace I Armijo ◽

Andrea S Vega ◽

Karem P Tamayo ◽

Diana E Gras ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Cell Division ◽

Root Growth ◽

Primary Root ◽

Growth Arrest ◽

Root Tip ◽

Wild Type ◽

Cytokinin Signaling ◽

Control Growth ◽

Primary Root Growth

Abstract Nitrate can act as a potent signal to control growth and development in plants. In this study, we show that nitrate is able to stimulate primary root growth via increased meristem activity and cytokinin signaling. Cytokinin perception and biosynthesis mutants displayed shorter roots as compared with wild-type plants when grown with nitrate as the only nitrogen source. Histological analysis of the root tip revealed decreased cell division and elongation in the cytokinin receptor double mutant ahk2/ahk4 as compared with wild-type plants under a sufficient nitrate regime. Interestingly, a nitrate-dependent root growth arrest was observed between days 5 and 6 after sowing. Wild-type plants were able to recover from this growth arrest, while cytokinin signaling or biosynthesis mutants were not. Transcriptome analysis revealed significant changes in gene expression after, but not before, this transition in contrasting genotypes and nitrate regimes. We identified genes involved in both cell division and elongation as potentially important for primary root growth in response to nitrate. Our results provide evidence linking nitrate and cytokinin signaling for the control of primary root growth in Arabidopsis thaliana.

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Conserved LBL1-ta-siRNA and miR165/166-RLD1/2 modules regulate root development in maize

Development ◽

10.1242/dev.190033 ◽

2020 ◽

Vol 148 (1) ◽

pp. dev190033

Author(s):

Vibhav Gautam ◽

Archita Singh ◽

Sandeep Yadav ◽

Sharmila Singh ◽

Pramod Kumar ◽

...

Keyword(s):

Root Growth ◽

Root Development ◽

Lateral Roots ◽

Root System Architecture ◽

Maize Root ◽

Altered Expression ◽

Auxin Distribution ◽

Seminal Roots ◽

Crown Roots

ABSTRACTRoot system architecture and anatomy of monocotyledonous maize is significantly different from dicotyledonous model Arabidopsis. The molecular role of non-coding RNA (ncRNA) is poorly understood in maize root development. Here, we address the role of LEAFBLADELESS1 (LBL1), a component of maize trans-acting short-interfering RNA (ta-siRNA), in maize root development. We report that root growth, anatomical patterning, and the number of lateral roots (LRs), monocot-specific crown roots (CRs) and seminal roots (SRs) are significantly affected in lbl1-rgd1 mutant, which is defective in production of ta-siRNA, including tasiR-ARF that targets AUXIN RESPONSE FACTOR3 (ARF3) in maize. Altered accumulation and distribution of auxin, due to differential expression of auxin biosynthesis and transporter genes, created an imbalance in auxin signalling. Altered expression of microRNA165/166 (miR165/166) and its targets, ROLLED1 and ROLLED2 (RLD1/2), contributed to the changes in lbl1-rgd1 root growth and vascular patterning, as was evident by the altered root phenotype of Rld1-O semi-dominant mutant. Thus, LBL1/ta-siRNA module regulates root development, possibly by affecting auxin distribution and signalling, in crosstalk with miR165/166-RLD1/2 module. We further show that ZmLBL1 and its Arabidopsis homologue AtSGS3 proteins are functionally conserved.

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The WUSCHELa (PtoWUSa) is Involved in Developmental Plasticity of Adventitious Root in Poplar

Genes ◽

10.3390/genes11020176 ◽

2020 ◽

Vol 11 (2) ◽

pp. 176 ◽

Cited By ~ 1

Author(s):

Jianbo Li ◽

Huixia Jia ◽

Pei Sun ◽

Jin Zhang ◽

Yongxiu Xia ◽

...

Keyword(s):

Cell Fate ◽

Apical Meristem ◽

Developmental Plasticity ◽

Profile Analysis ◽

Primary Root ◽

Ectopic Expression ◽

Populus Tomentosa ◽

Root Tip ◽

Expression Profile Analysis ◽

Auxin Transporter

WUSCHEL-RELATED HOMEOBOX (WOX) transcription factors play critical roles in cell fate determination during plant development. As the founding member of the WOX family, WUSCHEL (WUS) is characterized for its role in maintaining stem cell in meristem. In this study, we investigated the function of Populus tomentosa WUSCHELa (PtoWUSa) in adventitious roots (ARs) in poplar. Expression profile analysis showed that PtoWUSa was not only expressed in shoot apical meristem and stem, but also expressed in ARs. Ectopic expression of PtoWUSa in Arabidopsis resulted in shortened primary root, as well as agravitropism and multiple branches. Overexpression of PtoWUSa in poplar increased the number of ARs but decreased their length. Moreover, the AR tip and lateral root tip became larger and swollen. In addition, the expression of auxin transporter genes PIN-FORMED were downregulated in ARs of transgenic plant. Taken together, these results suggest that PtoWUSa could be involved in AR development in poplar through regulating the polar auxin transport in ARs.

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